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Dietary Diversity and Evolution of the Earliest Flying Vertebrates Revealed University of Birmingham Dietary diversity and evolution of the earliest flying vertebrates revealed by dental microwear texture analysis Bestwick, Jordan; Unwin, David; Butler, Richard; Purnell, Mark DOI: 10.1038/s41467-020-19022-2 License: Creative Commons: Attribution (CC BY) Document Version Publisher's PDF, also known as Version of record Citation for published version (Harvard): Bestwick, J, Unwin, D, Butler, R & Purnell, M 2020, 'Dietary diversity and evolution of the earliest flying vertebrates revealed by dental microwear texture analysis', Nature Communications, vol. 2020, 5293. https://doi.org/10.1038/s41467-020-19022-2 Link to publication on Research at Birmingham portal Publisher Rights Statement: Bestwick, J., Unwin, D.M., Butler, R.J. et al. Dietary diversity and evolution of the earliest flying vertebrates revealed by dental microwear texture analysis. Nat Commun 11, 5293 (2020). https://doi.org/10.1038/s41467-020-19022-2 General rights Unless a licence is specified above, all rights (including copyright and moral rights) in this document are retained by the authors and/or the copyright holders. The express permission of the copyright holder must be obtained for any use of this material other than for purposes permitted by law. •Users may freely distribute the URL that is used to identify this publication. •Users may download and/or print one copy of the publication from the University of Birmingham research portal for the purpose of private study or non-commercial research. •User may use extracts from the document in line with the concept of ‘fair dealing’ under the Copyright, Designs and Patents Act 1988 (?) •Users may not further distribute the material nor use it for the purposes of commercial gain. Where a licence is displayed above, please note the terms and conditions of the licence govern your use of this document. When citing, please reference the published version. Take down policy While the University of Birmingham exercises care and attention in making items available there are rare occasions when an item has been uploaded in error or has been deemed to be commercially or otherwise sensitive. If you believe that this is the case for this document, please contact [email protected] providing details and we will remove access to the work immediately and investigate. Download date: 01. Oct. 2021 ARTICLE https://doi.org/10.1038/s41467-020-19022-2 OPEN Dietary diversity and evolution of the earliest flying vertebrates revealed by dental microwear texture analysis ✉ ✉ Jordan Bestwick 1,2 , David M. Unwin3, Richard J. Butler 2 & Mark A. Purnell 1 Pterosaurs, the first vertebrates to evolve active flight, lived between 210 and 66 million years ago. They were important components of Mesozoic ecosystems, and reconstructing pter- 1234567890():,; osaur diets is vital for understanding their origins, their roles within Mesozoic food webs and the impact of other flying vertebrates (i.e. birds) on their evolution. However, pterosaur dietary hypotheses are poorly constrained as most rely on morphological-functional analo- gies. Here we constrain the diets of 17 pterosaur genera by applying dental microwear texture analysis to the three-dimensional sub-micrometre scale tooth textures that formed during food consumption. We reveal broad patterns of dietary diversity (e.g. Dimorphodon as a vertebrate consumer; Austriadactylus as a consumer of ‘hard’ invertebrates) and direct evi- dence of sympatric niche partitioning (Rhamphorhynchus as a piscivore; Pterodactylus as a generalist invertebrate consumer). We propose that the ancestral pterosaur diet was dominated by invertebrates and later pterosaurs evolved into piscivores and carnivores, shifts that might reflect ecological displacements due to pterosaur-bird competition. 1 Centre for Palaeobiology Research, School of Geography, Geology and the Environment, University of Leicester, Leicester LE1 7RH, UK. 2 School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK. 3 Centre for Palaeobiology Research, School of ✉ Museum Studies, University of Leicester, Leicester LE1 7RF, UK. email: [email protected]; [email protected] NATURE COMMUNICATIONS | (2020) 11:5293 | https://doi.org/10.1038/s41467-020-19022-2 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-020-19022-2 terosaurs, the first group of vertebrates to evolve active a range of different prey types. We also provide evidence of flight, lived between 210 and 66 million years ago during sympatric niche partitioning between Rhamphorhynchus and P 1 2 the Mesozoic . They had a global distribution and inhab- Pterodactylus, and evidence of ontogenetic niche partitioning in ited a range of terrestrial, coastal and marine environments3.As Rhamphorhynchus. Furthermore, we reconstruct pterosaur diet- important components of Mesozoic biotas4, robust reconstruc- ary evolution from our DMTA results by projecting pruned, time- tions of pterosaur diets are thus crucial not only for under- calibrated trees from three pterosaur phylogenies into the extant standing the ecological roles they performed within Mesozoic reptile multivariate framework, and by mapping pterosaur food webs, but for helping address broader ecological and evo- microwear characteristics from the reptile multivariate frame- lutionary debates that enhance our understanding of Mesozoic work onto each tree. We find that the diets of the first pterosaurs ecosystems. Key debates include: whether sympatric species of largely consisted of invertebrates and that pterosaurs became pterosaur competed for, or partitioned, food resources5; whether increasingly carnivorous and piscivorous over evolutionary time. ontogenetic stages of a single species competed for, or partitioned, These results provide insight into the multitude of roles that resources and thus had life-histories more similar to those of pterosaurs performed within Mesozoic food webs and highlight extant birds or non-avian reptiles6–8; and what impact the the applicability of DMTA for investigating extinct ecosystems. emergence and radiation of birds had on pterosaur dietary evo- 9 lution , and vice versa. Results and discussion Pterosaur diets have been the subject of considerable investi- Extant reptile and bat microwear frameworks. The extant rep- gation, but for many taxa there is little consensus regarding their tile framework comprises six crocodilian and seven monitor diet4. Dietary studies are inherently difficult because pterosaurs lizard species assigned to one of five dietary guilds: carnivores have no modern descendants10, and many dietary hypotheses are (tetrapod consumers); ‘harder’ invertebrate consumers (e.g. bee- based on weakly supported analogies between the morphology tles, crustaceans and shelled gastropods); ‘softer’ invertebrate and function of anatomical structures in extant animals and consumers (e.g. grasshoppers); omnivores; and piscivores (fish pterosaurs4. Fossilised stomach contents can be informative but consumers)18 (Supplementary Fig. 1 and Supplementary Data 1 are limited to a small number of specimens from a few species4,11. and 2). See Fig. 1a–f for examples of digital elevation models of Furthermore, studies that include dietary hypotheses typically extant reptile and pterosaur tooth surfaces from which texture focus on just one or two taxa, and the absence of a multi-taxon data were acquired. As previously reported18, four texture para- framework prevents reliable investigations into resource parti- meters differ significantly between reptile guilds (ANOVA; Sup- tioning between sympatric pterosaurs and the role of diet in plementary Data 3 and 4) and principal components analysis evolutionary transitions and responses to environmental separates them in a texture-dietary space defined by PC axes 1 upheavals12,13. and 2 (Fig. 2 and Supplementary Fig. 2). PC 1 negatively corre- A more robust approach to understanding diet involves dental lates with proportions of total vertebrates in reptile diets (r = microwear texture analysis (DMTA)—quantitative analysis of the s −0.3564, P = 0.0004) but positively correlates with total inver- sub-micrometre scale three-dimensional textures that form on – tebrates (r = 0.3192, P = 0.0016), while PC 2 positively correlates tooth surfaces during food consumption14 17. The difficulty s with dietary proportions of ‘softer’ invertebrates (r = 0.2907, P = experienced by consumers in piercing and chewing food items s 0.0043; Fig. 2; Supplementary Fig. 3 and Supplementary Data 5). determines the microwear patterns that form on tooth crowns In very broad terms, ‘harder’ foods correlate with rougher tex- which, consequently, provides direct evidence of diet18. Analyses tures, see ref. 18 for details). use standardised texture parameters14,19 to quantify microwear, The extant bat framework comprises eight species assigned to and thus dietary, differences between species and/or populations one of four guilds: carnivores; ‘harder’ invertebrate consumers; and therefore do not assume direct relationships between the piscivores; and ‘softest’ invertebrate (e.g. moths) consumers morphology and inferred functions of teeth14,15,17. Recent work (Supplementary Fig. 1, Supplementary Data 1 and 2 and has demonstrated that DMTA of non-occlusal (non-chewing) Supplementary Note 1). PCA of the 15 texture parameters that tooth surfaces of extant reptiles, including archosaurs (the clade significantly differ between guilds (Supplementary Data 3 and 4) to which
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